ICES Journal of Marine Science (2021), 78(1), 421–434. doi:10.1093/icesjms/fsaa043 Contribution to the Themed Section: ‘Marine aquaculture in the Anthropocene’ Food for Thought Downloaded from https://academic.oup.com/icesjms/article/78/1/421/5818947 by NOAA Central Library user on 06 April 2021 Moulding the ideal crab: implications of phenotypic plasticity for crustacean stock enhancement Benjamin J. Daly 1,*‡, Ginny L. Eckert 2, and W. Christopher Long 1 1Kodiak Laboratory, Resource Assessment and Conservation Engineering Division, Alaska Fisheries Science Center, National Marine Fisheries Service, NOAA, 301 Research Court, Kodiak, AK 99615, USA 2Juneau Center, College of Fisheries and Ocean Sciences, University of Alaska Fairbanks, 17101 Point Lena Loop Road, Juneau, AK 99801, USA *Corresponding author: tel: þ1 907 4861865; fax: þ1 907 4861824; e-mail: ben.daly@alaska.gov. Present address: Division of Commercial Fisheries, Alaska Department of Fish and Game, Westward Region, 351 Research Court, Kodiak, AK 99615, USA. Daly, B. J., Eckert, G. L., and Long, W. C. Moulding the ideal crab: implications of phenotypic plasticity for crustacean stock enhance- ment. – ICES Journal of Marine Science, 78: 421–434. Received 12 December 2019; revised 20 February 2020; accepted 21 February 2020; advance access publication 10 April 2020. Numerous examples of behavioural and morphological differences between hatchery-cultured and wild individuals exist for a range of crusta- cean species; however, we submit that these variances are not deficiencies, but rather are adaptive responses to an unnatural rearing environ- ment that may be detrimental in the natural environment. This phenotypic plasticity could be beneficial for stock enhancement because such plasticity suggests potential for change with adjustments to rearing protocols to achieve improved ecological competence. We examine how specific plastic responses can affect crustacean ecology through effects on predation, foraging, competition, and reproduction. For devel- oping stock enhancement programmes, we recommend consideration of plastic phenotypic patterns before large-scale releases are initiated. Researchers can identify environmental factors that cue plasticity during hatchery rearing, determine if induced responses are ecologically in- fluential after release into the wild, and examine the temporal scale on which phenotypic plasticity operates. Communal hatchery rearing at low-to-medium stocking densities with predator cues and natural substrates along with in situ conditioning, releases during periods of low predation risk, and coupled laboratory-field studies can contribute to improved ecological performance during stock enhancement. Finally, presentation of non-significant research results is needed to avoid bias towards hatchery–wild differences and help guide future conditioning programmes. Keywords: conditioning, ecological competence, phenotypic plasticity, release strategy, stock enhancement The need for aquaculture and stock enhancement large proportion of aquaculture is used for direct food produc- The expanding global human population has increased pressure tion (i.e. farming), improved culture technology has enabled the on wild fish stocks (Pauly et al., 1998; Pauly et al., 2002): 33% expansion of fisheries enhancement through the release of cul- of marine fish stocks are over-exploited (FAO, 2018). tured juveniles to augment wild populations (see Leber et al., Aquaculture could help meet future global fish demand in the 2004; Bell et al., 2005; Bell et al., 2006; Leber, 2013 for a review), face of constraints to capture fisheries expansion. Although a including cold water crustaceans (Nicosia and Lavalli, 1999; VC International Council for the Exploration of the Sea 2020. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is prop- erly cited. 422 B. J. Daly et al. Stevens et al., 2014). Wild releases of cultured juveniles have oc- marine crustaceans currently represent a relatively small propor- curred worldwide for a range of species and purposes with mixed tion of global aquaculture production (<1% by weight), they degrees of success. Generally, the goal of release efforts is to (i) re- comprise a significant proportion of economic value (2.3 billion place locally extinct populations (restocking), (ii) augment a nat- USD in 2017; FAO Global Aquaculture Production dataset). ural population where released individuals are harvested at a Advances in aquaculture technology have allowed for an increase larger size (“put and take” fisheries or sea ranching), or (iii) re- in the number of cultured crustacean species from 0 species/ build natural populations by overcoming recruitment limitation groups in 1980 to 41 species/groups in 2017 (FAO Global and bolstering the spawning stock (stock enhancement) (Leber, Aquaculture Production dataset); however, stock enhancement is 2013). not a new concept for marine crustaceans. Clawed lobsters were cultivated in Europe (Homarus gammarus) and North America Downloaded from https://academic.oup.com/icesjms/article/78/1/421/5818947 by NOAA Central Library user on 06 April 2021 The basis for stock enhancement for recruitment-limited (Homarus americanus) since the late 1800s (Beard et al., 1985; stocks Dannevig, 1885; Rathbun, 1886; Addison and Bannister, 1994; Aiken and Waddy, 1995; Bannister and Addison, 1998; Nicosia Stock enhancement works to bolster the spawning stock if the and Lavalli, 1999), and crab enhancement programmes have natural supply of juveniles is limited (Blankenship and Leber, emerged worldwide in recent decades (Ut, 2002; Obata et al., 1995), either from high natural mortality during the larval stages 2006; Cheng et al., 2008; Zohar et al., 2008; Lebata et al., 2009; or inadequate reproductive success (Bartley and Bell, 2008). Stevens et al., 2014). Still, marine invertebrate stock enhancement However, if substantial natural recruitment is present, density- has received less attention than finfish (Kitada and Kishino, dependent mortality may negate any benefits of stock enhance- 2006). Many crab and lobster wild capture fisheries have declined ment, especially if released individuals are too small to surpass over the past three decades (e.g. red king crab Paralithodes camt- conspecific predation bottlenecks (Lorenzen, 2005). In some schaticus, blue crab Callinectes sapidus, Australian spiny lobster cases, releases of cultured individuals can reduce the abundance Panulirus cygnus, Cape rock lobster Jasus lalandii). Small-scale en- of natural recruits through density-dependent processes resulting hancement efforts have been explored during times of localized in displacement of the natural population (Lorenzen et al., 2012). recruitment failure, even for species that experience high com- Furthermore, if factors such as limited habitat, food availability, mercial landings (e.g. American lobsters; Maine, USA; Beal and high predation pressure, or suboptimal adult or juvenile environ- Chapman, 2001; Beal, 2012 and references therein). mental conditions are the primary causes of low population Marine crustacean life history is favourable for stock enhance- abundances, then mortality in later juvenile or adult stages can ment efforts. High fecundity allows for large-scale hatchery pro- preclude successful stock enhancement. In the case of most har- duction that is orders of magnitude greater than for marine vested crustaceans, a spawner–recruit relationship is typically finfish (Kitada, 1999). Larvae survival is the most likely popula- very poor or non-existent, whereas, the juvenile–recruit relation- tion bottleneck for most crustacean species, and culturing larvae ship is often much more robust (Wahle, 2003). This suggests that in the hatchery could bypass this by eliminating or reducing mortality during the larval and settling stages is both high and many potential sources of natural mortality. For example, natural variable, whereas post-settling mortality is more predictable. This red king crab survival from hatching to the settling post-larval general pattern further suggests that crustaceans may be, in gen- stage is likely <1–2% (Shirley and Shirley, 1989) compared to eral, good candidates for stock enhancement when stocks are 50% survival in the hatchery (Swingle et al., 2013). Likewise, in depleted. the wild, blue crab larval survival was 0.16% to the settling stage Stock enhancement could be a powerful fishery management (McConaugha, 1992) compared to 43% survival in a hatchery or restoration tool to increase recruitment and smooth out highly (Zmora et al., 2005). The considerable improvement in hatchery stochastic recruitment trends and thereby increase either de- survival could be enough to allow released juveniles to overcome pressed populations or predictability in fisheries yields. Yet, the recruitment limitation. science behind stock enhancement is largely in its infancy (Molony et al., 2003; Leber, 2013), especially for marine inverte- Ecological competence brates (but see Bell et al., 2005 for a review). Most marine fish Crustacean stock enhancement programmes require production and invertebrate stocks display dramatic recruitment fluctuations, of millions of juveniles for use in large-scale releases (Aiken and likely caused by complex interactions among environmental con- Waddy, 1995; Bannister and Addison, 1998; Secor